Neurotrophins and their receptors in early development of the mammalian nervous system

Acta Neurobiologiae Experimentalis

Volumn 70, Issue 4, 2010, Pages 454-467

  Bartkowska, Katarzyna ^a   Turlejski, Kris ^a   Djavadian, Rouzanna L ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

BDNF; Developing brain; NGF; NT 3; NT 4 5; P75; Sortilin; TrkA; TrkB; TrkC

Indexed keywords

NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NERVOUS SYSTEM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MODELS, BIOLOGICAL; NERVE GROWTH FACTORS; NERVOUS SYSTEM; RECEPTORS, NERVE GROWTH FACTOR;

EID: 78951489453     PISSN: 00651400     EISSN: 00651400     Source Type: Journal    
DOI: None     Document Type: Article

References (120)

1. Alcántara S, Frisén J, del Río JA, Soriano E, Barbacid M, Silos-Santiago I (1997) TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced cell death. J Neurosci 17: 3623-3633.
2. Allendoerfer KL, Shelton DL, Shooter EM, Shatz CJ (1990) Nerve growth factor receptor immunoreactivity is transiently associated with the subplate neurons of the mammalian cerebral cortex. Proc Natl Acad Sci 87: 187-190.
3. Allendoerfer KL, Cabelli RJ, Escandón E, Kaplan DR, Nikolics K, Shatz CJ (1994) Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J Neurosci 14: 1795-1811.
4. Armanini MP, McMahon SB, Sutherland J, Shelton DL, Phillips HS (1995) Truncated and catalytic isoforms of trkB are co-expressed in neurons of rat and mouse CNS. Eur J Neurosci 7: 1403-1409.
5. Arevalo JC, Conde B, Hempstead BL, Chao MV, Martin-Zanca D, Perez P (2000) TrkA immunoglobulin-like ligand binding domains inhibit spontaneous activation of the receptor. Mol Cell Biol 20: 5908-5916.
6. Arumäe U, Pirvola U, Palgi J, Kiema TR, Palm K, Moshnyakov M, Ylikoski J, Saarma M (1993) Neurotrophins and their receptors in rat peripheral trigeminal system during maxillary nerve growth. J Cell Biol 122: 1053-1065.
7. Ayer-Lelievre CS, Ebendal T, Olson L, Seiger A (1983) Localization of nerve growth factor-like immunoreactivity in rat nervous tissue. Med Biol 61: 296-304.
8. Badowska-Szalewska E, Klejbor I, Cecot T, Spodnik JH, Moryś J (2009) Changes in NGF/c-Fos double staining in the structures of the limbic system in juvenile and aged rats exposed to forced swim test. Acta Neurobiol Exp (Wars) 69: 448-458.
9. Baker SA, Stanford LE, Brown RE, Hagg T (2005) Maturation but not survival of dopaminergic nigrostriatal neurons is affected in developing and aging BDNFdeficient mice. Brain Res 1039: 177-188.
10. Barde YA, Edgar D, Thoenen H (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J 1: 549-553.
11. Barnabé-Heider F and Miller FD (2003) Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 23: 5149-5160.
12. Barker PA, Lomen-Hoerth C, Gensch EM, Meakin SO, Glass DJ, Shooter EM (1993) Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J Biol Chem 268: 15150-15157.
13. Bartkowska K, Paquin A, Gauthier AS, Kaplan DR, Miller FD (2007) Trk signaling regulates neural precursor cellproliferation and differentiation during cortical development. Development 134: 4369-4380.
14. Baxter GT, Radeke MJ, Kuo RC, Makrides V, Hinkle B, Hoang R, Medina-Selby A, Coit D, Valenzuela P, Feinstein SC (1997) Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J Neurosci 17: 2683-2690.
15. Beltaifa S, Webster MJ, Ligons DL, Fatula RJ, Herman MM, Kleinman JE, Weickert CS (2005) Discordant changes in cortical TrkC mRNA and protein during the human lifespan. Eur J Neurosci 21: 2433-2444.
16. Bianchi LM, Conover JC, Fritzsch B, DeChiara T, Lindsay RM, Yancopoulos GD (1996) Degeneration of vestibular neurons in late embryogenesis of both heterozygous and homozygous BDNF null mutant mice. Development. 122: 1965-1973.
17. Buck CR, Martinez HJ, Black IB, Chao MV (1987) Developmentally regulated expression of the nerve growth factor receptor gene in the periphery and brain. Proc Natl Acad Sci 84: 3060-3063.
18. Carim-Todd L, Bath KG, Fulgenzi G, Yanpallewar S, Jing D, Barrick CA, Becker J, Buckley H, Dorsey SG, Lee FS, Tessarollo L (2009) Endogenous truncated TrkB.T1 receptor regulates neuronal complexity and TrkB kinase receptor function in vivo. J Neurosci 29: 678-685.
19. Chen EY, Mufson EJ, Kordower JH (1996) TRK and p75 neurotrophin receptor systems in the developing human brain. J Comp Neurol 369: 591-618.
20. Cheng A, Coksaygan T, Tang H, Khatri R, Balice-Gordon RJ, Rao MS, Mattson MP (2007) Truncated tyrosine kinase B brain-derived neurotrophic factor receptor directs cortical neural stem cells to a glial cell fate by a novel signaling mechanism. J Neurochem 100: 1515-1530.
21. Clary DO, Reichardt LF (1994) An alternatively spliced form of the nerve growth factor receptor TrkA confers an enhanced response to neurotrophin 3. Proc Natl Acad Sci 91: 11133-11137.
22. Cohen S, Levi-Montalcini R, Hamburger V (1954) A nerve growth-stimulating factor isolated from sarcomas 37 and 180. Proc Natl Acad Sci 40: 1014-1018.
23. Coulson EJ, Reid K, Shipham KM, Morley S, Kilpatrick TJ, Bartlett PF (2004) The role of neurotransmission and the Chopper domain in p75 neurotrophin receptor death signaling. Prog Brain Res 146: 41-62.
24. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts- Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, et al. (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76: 1001-1011.
25. Dubus P, Parrens M, El-Mokhtari Y, Ferrer J, Groppi A, Merlio JP (2000) Identification of novel trkA variants with deletions in leucine-rich motifs of the extracellular domain. J Neuroimmunol 107: 42-49.
26. Eide FF, Vining ER, Eide BL, Zang K, Wang XY, Reichardt LF (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16: 3123-3129.
27. Elkabes S, Dreyfus CF, Schaar DG, Black IB (1994) Embryonic sensory development: local expression of neurotrophin-3 and target expression of nerve growth factor J Comp Neurol 341: 204-213.
28. ElShamy WM, Linnarsson S, Lee KF, Jaenisch R, Ernfors P (1996) Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 122: 491-500.
29. Ernfors P, Hallböök F, Ebendal T, Shooter EM, Radeke MJ, Misko TP, Persson H (1988) Developmental and regional expression of beta-nerve growth factor receptor mRNA in the chick and rat. Neuron 1: 983-996.
30. Ernfors P, Merlio JP, Persson H (1992) Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4: 1140-1158.
31. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brainderived neurotrophic factor develop with sensory deficits. Nature 368: 147-150.
32. Ernfors P, Kucera J, Lee KF, Loring J, Jaenisch R (1995) Studies on the physiological role of brain-derived neurotrophic factor and neurotrophin-3 in knockout mice. Int J Dev Biol 39: 799-807.
33. Fagan AM, Garber M, Barbacid M, Silos-Santiago I, Holtzman DM (1997) A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo J Neurosci 17: 7644-7654.
34. Fariñas I, Jones KR, Backus C, Wang XY, Reichardt LF (1994) Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369: 658-661
35. Forooghian F, Kojic L, Gu Q, Prasad SS (2001) Identification of a novel truncated isoform of trkB in the kitten primary visual cortex. J Mol Neurosci 17: 81-88.
36. Fryer RH, Kaplan DR, Feinstein SC, Radeke MJ, Grayson DR, Kromer LF (1996) Developmental and mature expression of full-length and truncated TrkB receptors in the rat forebrain. J Comp Neurol 374: 21-40.
37. Fryer RH, Kaplan DR, Kromer LF (1997) Truncated trkB receptors on nonneuronal cells inhibit BDNF-induced neurite outgrowth in vitro. Exp Neurol 148: 616-627.
38. Fukumitsu H, Furukawa Y, Tsusaka M, Kinukawa H, Nitta A, Nomoto H, Mima T, Furukawa S, (1998) Simultaneous expression of brain-derived neurotrophic factor and neurotrophin-3 in Cajal-Retzius, subplate and ventricular progenitor cells during early development stages of the rat cerebral cortex. Neuroscience 84:115-127.
39. Götz R, Köster R, Winkler C, Raulf F, Lottspeich F, Schartl M, Thoenen H (1994) Neurotrophin-6 is a new member of the nerve growth factor family. Nature 372: 266-269.
40. Hallböök F (1999) Evolution of the vertebrate neurotrophin and Trk receptor gene families. Curr Opin Neurobiol 9: 616-621.
41. Hapner SJ, Boeshore KL, Large TH, Lefcort F (1998) Neural differentiation promoted by truncated trkC receptors in collaboration with p75(NTR). Dev Biol 201: 90-100.
42. Hayashi M, Mitsunaga F, Ohira K, Shimizu K, Yamashita A (1999) Development of full-length Trk B-immunoreactive structures in the hippocampal formation of the macaque monkey. Anat Embryol 199: 529-537.
43. Hayashi M, Mitsunaga F, Itoh M, Shimizu K, Yamashita A (2000) Development of full-length Trk B-immunoreactive structures in the prefrontal and visual cortices of the macaque monkey. Anat Embryol 201: 139-147.
44. Hempstead BL, Martin-Zanca D, Kaplan DR, Parada LF, Chao MV (1991) High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350: 678-683.
45. Hermans-Borgmeyer I, Hermey G, Nykjaer A, Schaller C (1999) Expression of the 100-kDa neurotensin receptor sortilin during mouse embryonal development. Brain Res Mol Brain Res 65: 216-219.
46. Holm PC, Rodríguez FJ, Kresse A, Canals JM, Silos-Santiago I, Arenas E (2003) Crucial role of TrkB ligands in the survival and phenotypic differentiation of developing locus coeruleus noradrenergic neurons. Development 130: 3535-3545.
47. Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642.
48. Huntley GW, Benson DL, Jones EG, Isackson PJ (1992) Developmental expression of brain derived neurotrophic factor mRNA by neurons of fetal and adult monkey prefrontal cortex. Brain Res Dev 70: 53-63.
49. Ibáñez CF, Ernfors P, Timmusk T, Ip NY, Arenas E, Yancopoulos GD, Persson H (1993) Neurotrophin-4 is a target-derived neurotrophic factor for neurons of the trigeminal ganglion. Development 117: 1345-1353.
50. Islam O, Loo TX, Heese K (2009) Brain-derived neurotrophic factor (BDNF) has proliferative effects on neural stem cells through the truncated TRK-B receptor, MAP kinase, AKT, and STAT-3 signaling pathways. Curr Neurovasc Res 6: 42-53.
51. Jahed A, Kawaja MD (2005) The influences of p75 neurotrophin receptor and brain-derived neurotrophic factor in the sympathetic innervation of target tissues during murine postnatal development. Auton Neurosci 118: 32-42.
52. Jansen P, Giehl K, Nyengaard JR, Teng K, Lioubinski O, Sjoegaard SS, Breiderhoff T, Gotthardt M, Lin F, Eilers A, Petersen CM, Lewin GR, Hempstead BL, Willnow TE, Nykjaer A (2007) Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat Neurosci 10: 1449-1457.
53. Jones KR, Fariñas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76: 989-999.
54. Kahn MA, Kumar S, Liebl D, Chang R, Parada LF, De Vellis J (1999) Mice lacking NT-3, and its receptor TrkC, exhibit profound deficiencies in CNS glial cells. Glia 26: 153-165.
55. Klein R (1994) Role of neurotrophins in mouse neuronal development. FASEB J 8: 738-744.
56. Klein R, Parada LF, Coulier F, Barbacid M (1989) TrkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J 8: 3701-3709.
57. Klein R, Martin-Zanca D, Barbacid M, Parada LF (1990) Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 109: 845-850.
58. Klein R, Smeyne RJ, Wurst W, Long LK, Auerbach BA, Joyner AL, Barbacid M (1993) Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death. Cell 75: 113-122.
59. Knüsel B, Rabin SJ, Hefti F, Kaplan DR (1994) Regulated neurotrophin receptor responsiveness during neuronal migrationand early differentiation. J Neurosci 14: 1542-1554.
60. Koh S, Loy R (1989) Localization and development of nerve growth factor-sensitive rat basal forebrain neurons and their afferent projections to hippocampus and neocortex. J Neurosci 9: 2999-3018.
61. Kordower JH, Mufson EJ (1992) Nerve growth factor receptor-immunoreactive neurons within the developing human cortex. J Comp Neurol 323: 25-41.
62. Kordower JH, Chen EY, Sladek JR Jr, Mufson EJ (1994) Trk-immunoreactivity in the monkey central nervous system: forebrain. J Comp Neurol 349: 20-35.
63. Lai KO, Fu WY, Ip FC, Ip NY (1998) Cloning and expression of a novel neurotrophin, NT-7, from carp. Mol Cell Neurosci 11: 64-76.
64. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69: 737-749.
65. Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948.
66. Levi-Montalcini R, Hamburger V (1951) Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 116: 321-361.
67. Liebl DJ, Tessarollo L, Palko ME, Parada LF (1997) Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice. J Neurosci 17: 9113-9121.
68. Liepinsh E, Ilag LL, Otting G, Ibáñez CF (1997) NMR structure of the death domain of the p75 neurotrophin receptor. EMBO J 16: 4999-5005.
69. Lotto RB, Asavaritikrai P, Vali L, Price DJ (2001) Targetderived neurotrophic factors regulate the death of developing forebrain neurons after a change in their trophic requirements. J Neurosci 21: 3904-3910.
70. Lu J, Wu Y, Sousa N, Almeida OF (2005) SMAD pathway mediation of BDNF and TGF beta 2 regulation of proliferation and differentiation of hippocampal granule neurons. Development 132: 3231-3242.
71. Luikart BW, Nef S, Shipman T, Parada LF (2003) In vivo role of truncated trkb receptors during sensory ganglion neurogenesis. Neuroscience 117: 847-858.
72. Luskin MB, Shatz CJ (1985) Neurogenesis of the cat's primary visual cortex. J Comp Neurol 242: 611-631.
73. Macias M (2008) Injury induced dendritic plasticity in the mature central nervous system. Acta Neurobiol Exp 68: 334-346.
74. Martin-Zanca D, Barbacid M, Parada LF (1990) Expression of the trk proto-oncogene is restricted to the sensory cranial and spinal ganglia of neural crest origin in mouse development. Genes Dev 4: 683-694.
75. Meinecke DL, Rakic P (1993) Low-affinity p75 nerve growth factor receptor expression in the embryonic monkey telencephalon: timing and localization in diverse cellular elements. Neuroscience 54: 105-116.
76. Menn B, Timsit S, Calothy G, Lamballe F (1998) Differential expression of TrkC catalytic and noncatalytic isoforms suggests that they act independently or in association J Comp Neurol 401: 47-64.
77. Mori T, Shimizu K, Hayashi M (2004) Differential expression patterns of TrkB ligands in the macaque monkey brain. Neuroreport 15: 2507-2511.
78. Mori T, Takumi K, Shimizu K, Oishi T, Hayashi M (2006) Heterogeneity of the developmental patterns of neurotrophin protein levels among neocortical areas of macaque monkeys. Exp Brain Res 171: 129-138.
79. Nakamura K, Namekata K, Harada C, Harada T (2007) Intracellular sortilin expression pattern regulates proNGFinduced naturally occurring cell death during development. Cell Death Differ 14: 1552-1554.
80. Numan S, Gall CM, Seroogy KB (2005) Developmental expression of neurotrophins and their receptors in postnatal rat ventral midbrain. J Mol Neurosci 27: 245-260.
81. Nykjaer A, Lee R, Teng KK, Jansen P, Madsen P, Nielsen MS, Jacobsen C, Kliemannel M, Schwarz E, Willnow TE, Hempstead BL, Petersen CM (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427: 843-848.
82. Ohira K, Shimizu K, Hayashi M (1999) Change of expression of full-length and truncated TrkBs in the developing monkey central nervous system. Brain Res Dev 112: 21-29.
83. Ohira K, Shimizu K, Hayashi M (2001) TrkB dimerization during development of the prefrontal cortex of the macaque. J Neurosci Res 65: 463-469.
84. Palko ME, Coppola V, Tessarollo L (1999) Evidence for a role of truncated trkC receptor isoforms in mouse development. J Neurosci 19: 775-782.
85. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306: 487-491.
86. Patel AV, Krimm RF (2010) BDNF is required for the survival of differentiated geniculate ganglion neurons. Dev Biol 340: 419-429.
87. Perez-Pinera P, García-Suarez O, Germanà A, Díaz-Esnal B, de Carlos F, Silos-Santiago I, del Valle ME, Cobo J, Vega JA (2008) Characterization of sensory deficits in TrkB knockout mice. Neurosci Lett 433: 43-47.
88. Peterson DA, Dickinson-Anson HA, Leppert JT, Lee KF, Gage FH (1999) Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. J Comp Neurol 404: 1-20.
89. Phillips HS, Hains JM, Laramee GR, Rosenthal A, Winslow JW (1990) Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons. Science 250: 290-294.
90. Piñon LG, Minichiello L, Klein R, Davies AM (1996) Timing of neuronal death in trkA, trkB and trkC mutant embryos reveals developmental changes in sensory neuron dependence on Trk signalling. Development 122: 3255-3261.
91. Pizzuti A, Borsani G, Falini A, Rugarli EI, Sidoli A, Baralle FE, Scarlato G, Silani V (1990) Detection of beta-nerve growth factor mRNA in the human fetal brain. Brain Res 518: 337-341.
92. Quartu M, Geic M, Del Fiacco M (1997) Neurotrophin-like immunoreactivity in the human trigeminal ganglion. Neuroreport 8: 3611-3617.
93. Quartu M, Lai ML, Del Fiacco M (1999) Neurotrophin-like immunoreactivity in the human hippocampal formation. Brain Res Bull 48: 375-382.
94. Quartu M, Serra MP, Manca A, Follesa P, Lai ML, Del Fiacco M (2003a) Neurotrophin-like immunoreactivity in the human pre-term newborn, infant, and adult cerebellum. Int J Dev Neurosci 21: 23-33.
95. Quartu M, Serra MP, Manca A, Follesa P, Ambu R, Del Fiacco M (2003b) High affinity neurotrophin receptors in the human pre-term newborn, infant, and adult cerebellum. Int J Dev Neurosci 21: 309-320.
96. Roux PP, Barker PA (2002) Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 67:203-233.
97. Schatteman GC, Gibbs L, Lanahan AA, Claude P, Bothwell M (1988) Expression of NGF receptor in the developing and adult primate central nervous system. J Neurosci 8: 860-873.
98. Schoups AA, Elliott RC, Friedman WJ, Black IB (1995) NGF and BDNF are differentially modulated by visual experience in the developing geniculocortical pathway. Brain Res Dev Brain Res 86: 326-334.
99. Schwartz PM, Borghesani PR, Levy RL, Pomeroy SL, Segal RA (1997) Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning. Neuron 19: 269-281.
100. Schweigreiter R (2006) The dual nature of neurotrophins. Bioessays 28: 583-594.
101. Seidah NG, Benjannet S, Pareek S, Savaria D, Hamelin J, Goulet B, Laliberte J, Lazure C, Chrétien M, Murphy RA (1996) Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem J 314: 951-960.
102. Shooter EM (2001) Early days of the nerve growth factor proteins. Annu Rev Neurosci 24: 601-629.
103. Silhol M, Bonnichon V, Rage F, Tapia-Arancibia L (2005) Agerelated changes in brain-derived neurotrophic factor and tyrosine kinase receptor isoforms in the hippocampus and hypothalamus in male rats. Neuroscience 132: 613-624.
104. Silos-Santiago I, Fagan AM, Garber M, Fritzsch B, Barbacid M (1997) Severe sensory deficits but normal CNS development in newborn mice lacking TrkB and TrkC tyrosine protein kinase receptors. Eur J Neurosci 9: 2045-2056.
105. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/ NGF receptor gene. Nature 368: 246-249.
106. Stoilov P, Castren E, Stamm S (2002) Analysis of the human TrkB gene genomic organization reveals novel TrkB isoforms, unusual gene length, and splicing mechanism. Biochem Biophys Res Commun 290: 1054-1065.
107. Tang S, Machaalani R, Waters KA (2010) Immunolocalization of pro- and mature-brain derived neurotrophic factor (BDNF) and receptor TrkB in the human brainstem and hippocampus. Brain Res 1354: 1-14.
108. Teng HK, Teng KK, Lee R, Wright S, Tevar S, Almeida RD, Kermani P, Torkin R, Chen ZY, Lee FS, Kraemer RT, Nykjaer A, Hempstead BL (2005) ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 25: 5455-5463.
109. Tessarollo L, Tsoulfas P, Martin-Zanca D, Gilbert DJ, Jenkins NA, Copeland NG, Parada LF (1993) TrkC, a receptor for neurotrophin-3, is widely expressed in the developing nervous system and in non-neuronal tissues. Development 118: 463-475.
110. Tessarollo L (1998) Pleiotropic functions of neurotrophins in development. Cytokine Growth Factor Rev 9: 125-137.
111. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270: 593-598.
112. Tsoulfas P, Stephens RM, Kaplan DR, Parada LF (1996) TrkC isoforms with inserts in the kinase domain show impaired signaling responses. J Biol Chem 271: 5691-5697.
113. Underwood CK, Coulson EJ (2008) The p75 neurotrophin receptor. Int J Biochem Cell Biol 40: 1664-1668.
114. Watson FL, Porcionatto MA, Bhattacharyya A, Stiles CD, Segal RA (1999) TrkA glycosylation regulates receptor localization and activity. J Neurobiol 39: 323-336.
115. Woolley AG, Tait KJ, Hurren BJ, Fisher L, Sheard PW, Duxson MJ (2008) Developmental loss of NT-3 in vivo results in reduced levels of myelin-specific proteins, a reduced extent of myelination and increased apoptosis of Schwann cells. Glia 56: 306-317.
116. Wyatt S, Davies AM (1993). Regulation of expression of mRNAs encoding the nerve growth factor receptors p75 and trkA in developing sensory neurons. Development 119: 635-648.
117. Valenzuela DM, Maisonpierre PC, Glass DJ, Rojas E, Nuñez L, Kong Y, Gies DR, Stitt TN, Ip NY, Yancopoulos GD (1993) Alternative forms of rat TrkC with different functional capabilities. Neuron 10: 963-974.
118. Yan Q, Johnson EM Jr (1988) An immunohistochemical study of the nerve growth factor receptor in developing rats. J Neurosci 8: 3481-398.
119. Yano H, Torkin R, Martin LA, Chao MV, Teng KK (2009) Proneurotrophin-3 is a neuronal apoptotic ligand: evidence for retrograde-directed cell killing. J Neurosci 29: 14790-14802.
120. Yeo TT, Chua-Couzens J, Butcher LL, Bredesen DE, Cooper JD, Valletta JS, Mobley WC, Longo FM (1997) Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J Neurosci 17: 7594-7605.